Diabetes onset influences hippocampal synaptic plasticity in streptozotocin-treated rats

Neuroscience

Volumn 227, Issue , 2012, Pages 293-304

  Sasaki Hamada, S ^a   Sacai, H ^a   Oka, J I ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

AMPA receptors; CA1; Diabetes; Hippocampal synaptic plasticity; NMDA receptors

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; INSULIN DEPENDENT DIABETES MELLITUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; RAT; STREPTOZOCIN DIABETES; SYNAPTIC TRANSMISSION;

AGE FACTORS; AGE OF ONSET; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; PICROTOXIN; RATS; RATS, WISTAR; REACTION TIME; RECEPTORS, GLUTAMATE; STREPTOZOCIN; SYNAPSES; VALINE;

EID: 84868529123     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.081     Document Type: Article

References (56)

1. Abraham W.C., Bear M.F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 1996, 19:126-130.
2. Ack M., Miller I., Weil W.B. Intelligence of children with diabetes mellitus. Pediatrics 1961, 28:764-770.
3. Artola A., Kamal A., Ramakers G.M., Biessels G.J., Gispen W.H. Diabetes mellitus concomitantly facilitates the induction of long-term depression and inhibits that of long-term potentiation in hippocampus. Eur J Neurosci 2005, 22:169-178.
4. Bear M.F., Abraham W.C. Long-term depression in hippocampus. Annu Rev Neurosci 1996, 19:437-462.
5. Bellone C., Nicoll R.A. Rapid bidirectional switching of synaptic NMDA receptors. Neuron 2007, 55:779-785.
6. Biessels G.J., Deary I.J., Ryan C.M. Cognition and diabetes: a lifespan perspective. Lancet Neurol 2008, 7:184-190.
7. Biessels G.J., Kamal A., Ramakers G.M., Urban I.J., Spruijt B.M., Erkelens D.W., Gispen W.H. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 1996, 45:1259-1266.
8. Bliss T.V., Collingridge G.L. Role of distinct NMDA receptor subtypes at central synapses. Nature 1993, 361:31-39.
9. Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973, 232:331-356.
10. Bredt D.S., Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 2003, 40:361-379.
11. Caporale N., Dan Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 2008, 31:25-46.
12. Chabot C., Massicotte G., Milot M., Trudeau F., Gagné J. Impaired modulation of AMPA receptors by calcium-dependent processes in streptozotocin-induced diabetic rats. Brain Res 1997, 768:249-256.
13. Collingridge G.L., Isaac J.T., Wang Y.T. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 2004, 5:952-962.
14. 2+ signaling requirements for long-term depression in the hippocampus. Neuron 1996, 16:825-833.
15. Daneman D. Type 1 diabetes. Lancet 2006, 367:847-858.
16. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
17. Di Luca M., Ruts L., Gardoni F., Biessels G.J., Gispen W.H. NMDA receptor subunit are modified trascriptionally and post-translationally in the brain of streptozotocin-diabeteic rats. Diabetologia 1999, 42:693-701.
18. Dudek S.M., Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade. Proc Natl Acad Sci U S A 1992, 89:4363-4367.
19. Dudek S.M., Bear M.F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 1993, 13:2910-2918.
20. Ferguson S.C., Blane A., Wardlow J., Ferier B.M., Perros P., McCrimmon R.J., Deary I.J. Influence of an early-onset age of type 1 diabetes on cerebral structure and cognitive function. Diabetes Care 2005, 28:1431-1437.
21. Gardoni F., Kamal A., Bellone C., Biessels G.J., Ramakers G.M., Cattabeni F., Gispen W.H., Di Luca M. Effects of streptozotocin-diabetes on the hippocample NMDA receptor complex in rats. J Neurochem 2002, 80:438-447.
22. Gaudieri P.A., Chen R., Greer T.F., Holmes C.S. Cognitive function in children with type 1 diabetes. Diabetes Care 2008, 31:1892-1897.
23. Heng L.J., Yang R.H., Jia D. Diabetes impairs learning performance through affecting membrane excitability of hippocampal pyramidal neurons. Behav Brain Res 2011, 224:250-258.
24. Holmes C.S., Richman L.C. Cognitive profiles of children with insulin-dependent diabetes. J Dev Behav Pediatr 1985, 6:323-326.
25. Iwai T., Suzuki M., Kobayashi K., Mori K., Mogi Y., Oka J.-I. The influence of juvenile diabetes on memory and hippocampal plasticity in rats: improving effects of glucagon-like peptide-1. Neurosci Res 2009, 64:67-74.
26. Kamal A., Biessels G.J., Duis S.E., Gispen W.H. Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing. Diabetologia 2000, 43:500-506.
27. Kamal A., Biessels G.J., Gispen W.H., Ramakers G.M. Synaptic transmission changes in the pyramidal cells of the hippocampus in streptozotocin-induced diabetes mellitus in rats. Brain Res 2006, 1073-1074:276-280.
28. Kamal A., Biessels G.J., Urban I.J., Gispen W.H. Hippocampal synaptic plasticity in streptozotocin-diabetic rats: impairment of long-term potentiation and facilitation of long-term depression. Neuroscience 1999, 90:737-745.
29. Kampa B.M., Letzkus J.J., Stuart G.J. Dendritic mechanisms controlling spike-timing-dependent synaptic plasticity. Trends Neurosci 2007, 30:456-463.
30. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294:1030-1038.
31. Katz B., Miledi R. The role of calcium in neuromuscular facilitation. J Physiol 1968, 195:481-492.
32. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 2002, 3:453-462.
33. Liu L., Wong T.P., Pozza M.F., Lingenhoehl K., Wang Y., Sheng M., Auberson Y.P., Wang Y.T. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 2004, 304:1021-1024.
34. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
35. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25:103-126.
36. McEwen B.S. Stress and hippocampal plasticity. Annu Rev Neurosci 1999, 22:105-122.
37. Mulkey R.M., Malenka R.C. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 1992, 9:967-975.
38. Nishiyama M., Hong K., Mikoshiba K., Poo M.M., Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 2000, 408:584-588.
39. Norris C.M., Korol D.L., Foster T.C. Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J Neurosci 1996, 16:5382-5392.
40. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 1992, 106:62-71.
41. Pavlides C., Ogawa S., Kimura A., McEwen B.S. Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices. Brain Res 1996, 738:229-235.
42. Petralia R.S., Esteban J.A., Wang Y.X., Partridge J.G., Zhao H.M., Wenthold R.J., Malinow R. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 1999, 2:31-36.
43. Piotrowski P., Wierzbicka K., Smiałek M. Neuronal death in the rat hippocampus in experimental diabetes and cerebral ischaemia treated with antioxidants. Folia Neuropathol 2001, 39:147-154.
44. Popoli M., Yan Z., McEwen B.S., Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 2011, 13:22-37.
45. Revsin Y., Rekers N.V., Louwe M.C., Saravia F.E., De Nicola A.F., de Kloet E.R., Oitzl M.S. Glucocorticoid receptor blockade normalizes hippocampal alterations and cognitive impairment in streptozotocin-induced type 1 diabetes mice. Neuropsychopharmacology 2009, 34:747-758.
46. Ryan C., Vega A., Drash A. Cognitive deficits in adolescents who developed diabetes early in life. Pediatrics 1985, 75:921-927.
47. Sandler V.M., Ross W.N. Serotonin modulates spike backpropagation and associated [Ca2+]i changes in the apical dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 1999, 81:216-224.
48. Selig D.K., Hjelmstad G.O., Herron C., Nicoll R.A., Malenka R.C. Independent mechanisms for long-term depression of AMPA and NMDA responses. Neuron 1995, 15:417-426.
49. Shors T.J., Seib T.B., Levine S., Thompson R.F. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 1989, 244:224-226.
50. Stranahan A.M., Arumugam T.V., Cutler R.G., Lee K., Egan J.M., Mattson M.P. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 2008, 11:309-317.
51. Tsubokawa H., Ross W.N. Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 1997, 17:5782-5791.
52. Wagner J.J., Alger B.E. GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus. J Neurosci 15, 1577-1586. J Neurosci 1995, 15:1577-1586.
53. Wu G., Malinow R., Cline H.T. Maturation of a central glutamatergic synapse. Science 1996, 274:972-976.
54. Xu L., Anwyl R., Rowan M.J. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 1997, 387:497-500.
55. Ye L., Wang F., Yang R.H. Diabetes impairs learning performance and affects the mitochondrial function of hippocampal pyramidal neurons. Brain Res 2011, 1411:57-64.
56. Zucker R.S. Short-term synaptic plasticity. Annu Rev Neurosci 1989, 12:13-31.